Showing papers by "Bo Thamdrup published in 2018"

Conductive Particles Enable Syntrophic Acetate Oxidation between Geobacter and Methanosarcina from Coastal Sediments

Abstract: Coastal sediments are rich in conductive particles, possibly affecting microbial processes for which acetate is a central intermediate. In the methanogenic zone, acetate is consumed by methanogens and/or syntrophic acetate-oxidizing (SAO) consortia. SAO consortia live under extreme thermodynamic pressure, and their survival depends on successful partnership. Here, we demonstrate that conductive particles enable the partnership between SAO bacteria (i.e., Geobacter spp.) and methanogens (Methanosarcina spp.) from the coastal sediments of the Bothnian Bay of the Baltic Sea. Baltic methanogenic sediments were rich in conductive minerals, had an apparent isotopic fractionation characteristic of CO2-reductive methanogenesis, and were inhabited by Geobacter and Methanosarcina As long as conductive particles were delivered, Geobacter and Methanosarcina persisted, whereas exclusion of conductive particles led to the extinction of Geobacter Baltic Geobacter did not establish a direct electric contact with Methanosarcina, necessitating conductive particles as electrical conduits. Within SAO consortia, Geobacter was an efficient [13C]acetate utilizer, accounting for 82% of the assimilation and 27% of the breakdown of acetate. Geobacter benefits from the association with the methanogen, because in the absence of an electron acceptor it can use Methanosarcina as a terminal electron sink. Consequently, inhibition of methanogenesis constrained the SAO activity of Geobacter as well. A potential benefit for Methanosarcina partnering with Geobacter is that together they competitively exclude acetoclastic methanogens like Methanothrix from an environment rich in conductive particles. Conductive particle-mediated SAO could explain the abundance of acetate oxidizers like Geobacter in the methanogenic zone of sediments where no electron acceptors other than CO2 are available.IMPORTANCE Acetate-oxidizing bacteria are known to thrive in mutualistic consortia in which H2 or formate is shuttled to a methane-producing Archaea partner. Here, we discovered that such bacteria could instead transfer electrons via conductive minerals. Mineral SAO (syntrophic acetate oxidation) could be a vital pathway for CO2-reductive methanogenesis in the environment, especially in sediments rich in conductive minerals. Mineral-facilitated SAO is therefore of potential importance for both iron and methane cycles in sediments and soils. Additionally, our observations imply that agricultural runoff or amendments with conductive chars could trigger a significant increase in methane emissions.

Denitrification, anaerobic ammonium oxidation, and dissimilatory nitrate reduction to ammonium in an East African Great Lake (Lake Kivu).

Abstract: We investigated anaerobic nitrogen (N) cycling in the water column of Lake Kivu, a deep meromictic tropical lake in East Africa. Data were collected at one station in the Northern Basin and one in the Southern Basin, during two sampling campaigns (June 2011—dry season, and February 2012—rainy season). Short-term incubations of sulfide-free water with 15N-labeled substrates revealed high potential denitrification and dissimilatory nitrate reduction to ammonium (DNRA) rates (up to 350 and 36 nmol N produced L−1 h−1, respectively), while anaerobic ammonium oxidation (anammox) was lower (up to 3.3 nmol N produced L−1 h−1). However, anammox rates were 15 nmol N produced L−1 h−1 when 15 NH4+ was added at depths where NH4+ concentrations were very low (< 1 μmol L−1). With the addition of 5 μmol L−1 of 15 NO3− and 10 μmol L−1 of H2S, denitrification and anammox were stimulated in the Northern Basin, while the increase of DNRA rates was less notable. In the Southern Basin, the addition of H2S decreased denitrification rates, probably because of competition with DNRA, which increased, while no effect was observed on anammox. This study puts into evidence the co-occurrence of denitrification, anammox and DNRA, for the first time in a great tropical lake, and underlines the spatial heterogeneity of these processes. Contrary to numerous reports in literature, we show that anammox can significantly occur in presence of H2S, suggesting that the contribution of anammox in the N cycle may be underestimated.

Single cell genomic and transcriptomic evidence for the use of alternative nitrogen substrates by anammox bacteria

Abstract: Anaerobic ammonium oxidation (anammox) contributes substantially to ocean nitrogen loss, particularly in anoxic marine zones (AMZs). Ammonium is scarce in AMZs, raising the hypothesis that organic nitrogen compounds may be ammonium sources for anammox. Biochemical measurements suggest that the organic compounds urea and cyanate can support anammox in AMZs. However, it is unclear if anammox bacteria degrade these compounds to ammonium themselves, or rely on other organisms for this process. Genes for urea degradation have not been found in anammox bacteria, and genomic evidence for cyanate use for anammox is limited to a cyanase gene recovered from the sediment bacterium Candidatus Scalindua profunda. Here, analysis of Ca. Scalindua single amplified genomes from the Eastern Tropical North Pacific AMZ revealed genes for urea degradation and transport, as well as for cyanate degradation. Urease and cyanase genes were transcribed, along with anammox genes, in the AMZ core where anammox rates peaked. Homologs of these genes were also detected in meta-omic datasets from major AMZs in the Eastern Tropical South Pacific and Arabian Sea. These results suggest that anammox bacteria from different ocean regions can directly access organic nitrogen substrates. Future studies should assess if and under what environmental conditions these substrates contribute to the ammonium budget for anammox.

N2 production through denitrification and anammox across the continental margin (shelf-slope-rise) of the Ulleung Basin, East Sea

Abstract: Experimental determinations of nitrogen cycling in deep-sea sediments are strongly underrepresented in the databases. To investigate the total N2 production rates and relative contribution of denitrification and anaerobic ammonium oxidation (anammox) to benthic fixed-N removal processes, we conducted N isotope-labeling incubation experiments in whole cores and slurries at nine stations across the continental margin from the shelf (< 200 m) and into the deep (> 2000 m) Ulleung Basin (UB) in the East Sea. The total N2 production rates (anammox plus denitrification) in the center of the UB (8.4 6 0.2 lmol N m 22 h) were high compared to most other deep-sea sediments at similar water depths. Denitrification rates decreased from the shelf (7.6 6 0.6 lmol N m h) to the basin (3.2 6 0.4 lmol N m h), in proportion to benthic oxygen consumption, whereas anammox rates remained relatively constant or even increased slightly (1.3– 4.1 lmol N m h). The contribution of anammox to the total N2 production (ra) increased with increasing water depth from the shelf (ca. 17%) to the basin (ca. 56%). The enhanced ra in the center of the UB was associated with an increased availability of nitrite for anammox, which was likely a result of the competitive suppression of denitrification by manganese reduction under MnO2-rich conditions. Our results emphasize the importance of anammox as a sink for reactive nitrogen in deep-sea sediments and contribute toward a mechanistic understanding of the factors controlling benthic reactive nitrogen loss in the ocean. Approximately 50–70% of the removal of fixed nitrogen from the oceans is estimated to occur in organic-rich sediments deposited on the continental margins including shelf, slope, and rise (Codispoti et al. 2001; de Vries et al. 2013). Here, fixed N is transformed into inert dinitrogen gas (N2) by the two anaerobic microbial processes; denitrification and anammox. Denitrification is a respiratory process whereby nitrate is used as the terminal electron acceptor in the oxidation of either organic matter (5CH2O 1 4NO 2 3 ! 5CO2 1 2N2 1 7H2O) or inorganic compounds including hydrogen, ferrous iron, or reduced sulfur compounds (Straub et al. 1996; Zumft 1997). During anammox (short for anaerobic ammonium oxidation), NO2 is utilized as an electron acceptor to oxidize NH4 (NH 1 4 1 NO 2 2 ! N2 1 2H2O; Van De Graaf et al. 1995). The average relative contribution of anammox to marine benthic N2 production is estimated to 28% (Trimmer and Engstr€ om 2011). The contribution varies widely, however, with anammox being almost insignificant in many shallow coastal locations while it dominates as N2 source in some deeper sediments, particularly. This apparent dependence on water depth is mainly driven by decreasing denitrification rates with increasing water depth while anammox rates show lower variability (Dalsgaard et al. 2005; Trimmer and Engstr€ om 2011). The decrease in denitrification activity with increasing depth is attributed to a concurrent decrease in the availability of organic carbon (Thamdrup and Dalsgaard 2002; Engstr€ om et al. 2005), whereas various factors (i.e., temperature, bottom water NO3 concentration, and organic carbon content) have been considered to regulate the anammox process (Risgaard-Petersen et al. 2004; Trimmer and Nicholls 2009). *Correspondence: hyunjh@hanyang.ac.kr Additional Supporting Information may be found in the online version of this article. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. S410 LIMNOLOGY and OCEANOGRAPHY Limnol. Oceanogr. 63, 2018, S410–S424 VC 2017 The Authors Limnology and Oceanography published by Wiley Periodicals, Inc. on behalf of Association for the Sciences of Limnology and Oceanography doi: 10.1002/lno.10750

Effect of settled diatom-aggregates on benthic nitrogen cycling

Abstract: The marine sediment hosts a mosaic of microhabitats. Recently it has been demonstrated that the settlement of phycodetrital aggregates can induce local changes in the benthic O2 distribution due to confined enrichment of organic material and alteration of the diffusional transport. Here, we show how this microscale O2 shift substantially affects benthic nitrogen cycling. In sediment incubations, the settlement of diatom-aggregates markedly enhanced benthic O2 and NO3- consumption and stimulated NO2- and NH4+ production. Oxygen microprofiles revealed the rapid development of anoxic niches within and underneath the aggregates. During 120 h following the settling of the aggregates, denitrification of NO3- from the overlying water increased from 13.5 μmol m-2 h-1 to 24.3 μmol m-2 h-1, as quantified by 15N enrichment experiment. Simultaneously, N2 production from coupled nitrification-denitrification decreased from 33.4 μmol m-2 h-1 to 25.9 μmol m-2 h-1, probably due to temporary inhibition of the benthic nitrifying community. The two effects were of similar magnitude and left the total N2 production almost unaltered. At the aggregate surface, nitrification was, conversely, very efficient in oxidizing NH4+ liberated by mineralization of the aggregates. The produced NO3- was preferentially released into the overlying water and only a minor fraction contributed to denitrification activity. Overall, our data indicate that the abrupt change in O2 microdistribution caused by aggregates stimulates denitrification of NO3- from the overlying water, and loosens the coupling between benthic nitrification and denitrification both in time and space. The study contributes to expanding the conceptual and quantitative understanding of how nitrogen cycling is regulated in dynamic benthic environments.

Interspecies interactions mediated by conductive minerals in the sediments of the ferruginous Lake La Cruz, Spain

Abstract: Lake La Cruz is considered a biogeochemical analogue to early Earth marine environments because its water column is depleted in sulfate, but rich in methane and iron, similar to conditions envisaged for much of the Precambrian. In this early Earth analogue environment, we show that conductive particles establish a tight metabolic coupling between electroactive microbial clades. We propose that mineral-based syntrophy is of potential relevance for the evolution of Earth9s earliest complex life forms. We show that the anoxic sediment of Lake La Cruz, which is rich in biogeochemically reactive iron minerals, harbors known electroactive species such as Geobacter and Methanothrix , in addition to other groups which have not been previously associated with an electroactive lifestyle. Slurry incubations on various substrates in the presence of conductive particles showed significant methanogenic activity, whereas incubations with non-conductive glass beads resulted in low methanogenic rates similar to slurries without added particles. In the absence of conductive particles, all tested substrates were metabolized to acetate, which accumulated to ~10 mM. Similar to a previous study on iron-rich Baltic Sea sediments, we observed that conductive mineral additions to La Cruz slurries enabled acetate oxidation, thus preventing acetate accumulation. Acetate oxidation coupled to high methanogenic activity was only maintained in successive mud-free enrichments when these were amended with conductive minerals. In serial mud-free transfers, conductive particles conserved a consortium of Youngiibacter-Methanothrix , whereas Youngiibacter spp. died off in the absence of conductive particles. In contrast, mud-free enrichments without conductive particles ceased any metabolic activity during the second transfers. Syntrophic consortia from this early Earth analogue environment only survived in the presence of conductive particles. Mineral-mediated syntrophy could be one of the earliest evolutionary interspecies associations. Conductive minerals might have fueled metabolic exchange between cells via intercellular electron transfer prompting tight cell-to-cell associations and possibly eukaryogenesis.

Extracellular Electron Uptake by Two Methanosarcina Species

Abstract: Direct electron uptake by prokaryotes is a recently described mechanism with a potential application for energy and CO2 storage into value added chemicals. Members of Methanosarcinales, an environmentally and biotechnologically relevant group of methanogens, were previously shown to retrieve electrons from an extracellular electrogenic partner performing Direct Interspecies Electron Transfer (DIET) and were therefore proposed to be electroactive. However, their intrinsic electroactivity has never been examined. In this study, we tested two methanogens belonging to Methanosarcina, M. barkeri and M. horonobensis, regarding their ability to accept electrons directly from insoluble electron donors like other cells, conductive particles and electrodes. Both methanogens were able to retrieve electrons from Geobacter metallireducens via DIET. Furthermore, DIET was also stimulated upon addition of electrically conductive granular activated carbon (GAC) when each was co-cultured with G. metallireducens. However, when provided with a cathode poised at - 400 mV (vs SHE), only M. barkeri could perform electromethanogenesis. In contrast, the strict hydrogenotrophic methanogen, Methanobacterium formicicum, did not produce methane regardless of the type of insoluble electron donor provided (Geobacter cells, GAC or electrodes). A comparison of functional gene categories between Methanobacterium and the two Methanosarcinas revealed a higher abundance of genes associated with extracellular electron transfer in Methanosarcina species. Between the two Methanosarcina we observed differences regarding energy metabolism, which could explain dissimilarities concerning electromethanogenesis at fixed potentials. We suggest that these dissimilarities are minimized in the presence of an electrogenic DIET partner (i.e. Geobacter), which can modulate its surface redox potentials by adjusting the expression of electroactive surface proteins.

Diagnostics, Monitoring and Mitigation of N2O Emissions from Wastewater Treatment Operations – Outcomes of the LAGAS project

Abstract: In the later years, significant focus has been placed on spin-outs and commercialization of research from the universities. Working in this tension field between high-level research and commercialization can be difficult and to be successful many barriers at the universities and in the commercial world has to be crossed, while balancing expectations from both worlds. Our background is a large research group working with geophysical methods for high-resolution characterization of the shallow subsurface where most of the human activities take place. Like CRT scanners provide insight into the hidden parts of the human body in the medical world we provide electromagnetic scans of the hidden underground. This information is used in different areas like farming, construction, water exploration etc. We are in many ways very successful and run a research group of about 20 people all driven by various sources of external funding. In this presentation, we discuss barriers between the research world, the commercial world and the expectations from the funding agencies. This is based on experience from a number of large national as well as international research projects. We have also created several spin-out companies from the research group, a process which is much more difficult than often communicated from the political system. * esben.auken@geo.au.dk, CF Møllers Alle 4, bygn. 1120, 8000 Aarhus C ** anders.vest@geo.au.dk, CF Møllers Alle 4, bygn. 1120, 8000 Aarhus C